Non-invasive, Brain-controlled Functional Electrical Stimulation for Locomotion Rehabilitation in Individuals with Paraplegia
Open accessAbstract
Spinal cord injury (SCI) impairs the flow of sensory and motor signals between the brain and the areas of the body located below the lesion level. Here, we describe a neurorehabilitation setup combining several approaches that were shown to have a positive effect in patients with SCI: gait training by means of non-invasive, surface functional electrical stimulation (sFES) of the lower-limbs, proprioceptive and tactile feedback, balance control through overground walking and cue-based decoding of cortical motor commands using a brain-machine interface (BMI). The central component of this new approach was the development of a novel muscle stimulation paradigm for step generation using 16 sFES channels taking all sub-phases of physiological gait into account. We also developed a new BMI protocol to identify left and right leg motor imagery that was used to trigger an sFES-generated step movement. Our system was tested and validated with two patients with chronic paraplegia. These patients were able to walk safely with 65–70% body weight support, accumulating a total of 4,580 steps with this setup. We observed cardiovascular improvements and less dependency on walking assistance, but also partial neurological recovery in both patients, with substantial rates of motor improvement for one of them.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Brain-controlled neuromuscular stimulation also mediated durable functional improvements of the engaged muscles after stroke and spinal cord injury.
“Brain-controlled neuromuscular stimulation also mediated durable functional improvements of the engaged muscles after stroke36 and spinal cord injury22,24,37.”
From Walking naturally after spinal cord injury using a brain–spine interface (2023) · cites this paper as [24]
The Results (Clinical improvements; page unavailable) report improved motor function in stimulated muscles of two patients with spinal cord injury, assessed without stimulation after training. The paper does not establish that those improvements persisted over a longer follow-up period, so the claim of durability is not supported by this source. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
A review of classification algorithms for EEG-based brain–computer interfaces
Lotte, F., Congedo, M., Lécuyer, A., Lamarche, F., & Arnaldi, B. (2007) · Journal of Neural Engineering · doi:10.1088/1741-2560/4/2/r01 · Cited by 2,665 · see citing works
Optimal spatial filtering of single trial EEG during imagined hand movement
Ramoser, H., Muller-Gerking, J., & Pfurtscheller, G. (2000) · IEEE Transactions on Rehabilitation Engineering · doi:10.1109/86.895946 · Cited by 2,457 · see citing works
International standards for neurological classification of spinal cord injury (Revised 2011)
Kirshblum, S. C., Burns, S. P., Biering-Sorensen, F., Donovan, W., Graves, D. E., Jha, A., Johansen, M., Jones, L., Krassioukov, A., Mulcahey, M. J., et al. (2011) · The Journal of Spinal Cord Medicine · doi:10.1179/204577211x13207446293695 · Cited by 2,327 · see citing works
Motor imagery and direct brain-computer communication
Pfurtscheller, G., & Neuper, C. (2001) · Proceedings of the IEEE · doi:10.1109/5.939829 · Cited by 1,990 · see citing works
Cappozzo, A., Catani, F., Croce, U. D., & Leardini, A. (1995) · Clinical Biomechanics · doi:10.1016/0268-0033(95)91394-t · Cited by 1,677 · see citing works
Repeatability of kinematic, kinetic, and electromyographic data in normal adult gait
Kadaba, M. P., Ramakrishnan, H. K., Wootten, M. E., Gainey, J., Gorton, G. E., & Cochran, G. V. B. (1989) · Journal of Orthopaedic Research® · doi:10.1002/jor.1100070611 · Cited by 1,479 · see citing works
Brain–machine interface in chronic stroke rehabilitation: A controlled study
Ramos‐Murguialday, A., Broetz, D., Rea, M., Läer, L., Yilmaz, Ö., Brasil, F. L., Liberati, G., Curado, M. R., García‐Cossio, E., Vyziotis, A., et al. (2013) · Annals of Neurology · doi:10.1002/ana.23879 · Cited by 994 · see citing works
Esquenazi, A., Talaty, M., Packel, A., & Saulino, M. (2012) · American Journal of Physical Medicine & Rehabilitation · doi:10.1097/phm.0b013e318269d9a3 · Cited by 958 · see citing works
Fawcett, J. W., Curt, A. E. P., Steeves, J. D., Coleman, W. P., Tuszynski, M. H., Lammertse, D. P., Bartlett, P. F., Blight, A. R., Dietz, V., Ditunno, J. F., et al. (2006) · Spinal Cord · doi:10.1038/sj.sc.3102007 · Cited by 882 · see citing works
Ajiboye, A. B., Willett, F. R., Young, D. R., Memberg, W. D., Murphy, B. A., Miller, J. P., Walter, B. L., Sweet, J. A., Hoyen, H. A., Keith, M. W., et al. (2017) · The Lancet · doi:10.1016/s0140-6736(17)30601-3 · Cited by 862 · see citing works
Renard, Y., Lotte, F., Gibert, G., Congedo, M., Maby, E., Delannoy, V., Bertrand, O., & Lécuyer, A. (2010) · Presence: Teleoperators and Virtual Environments · doi:10.1162/pres.19.1.35 · Cited by 830 · see citing works
EMG profiles during normal human walking: stride-to-stride and inter-subject variability
Winter, D. A., & Yack, H. J. (1987) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(87)90003-4 · Cited by 681 · see citing works
Brain-Machine Interfaces: From Basic Science to Neuroprostheses and Neurorehabilitation
Lebedev, M., & Nicolelis, M. A. L. (2017) · Physiological Reviews · doi:10.1152/physrev.00027.2016 · Cited by 655 · see citing works
Self-citationBrain-actuated functional electrical stimulation elicits lasting arm motor recovery after stroke
Biasiucci, A., Leeb, R., Iturrate, I., Perdikis, S., Al-Khodairy, A., Corbet, T., Schnider, A., Schmidlin, T., Zhang, H., Bassolino, M., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-04673-z · Cited by 649 · see citing works
A brain–spine interface alleviating gait deficits after spinal cord injury in primates
Capogrosso, M., Milekovic, T., Borton, D., Wagner, F., Moraud, E. M., Mignardot, J.-B., Buse, N., Gandar, J., Barraud, Q., Xing, D., et al. (2016) · Nature · doi:10.1038/nature20118 · Cited by 635 · see citing works
Recruitment Patterns in Human Skeletal Muscle During Electrical Stimulation
Gregory, C. M., & Bickel, C. S. (2005) · Physical Therapy · doi:10.1093/ptj/85.4.358 · Cited by 615 · see citing works
Kirshblum, S., Waring, W. P., Biering‐Sørensen, F., Burns, S. P., Johansen, M., Schmidt-Read, M., Donovan, W. H., Graves, D. E., Jha, A., Jones, L., et al. (2011) · Journal of Spinal Cord Medicine · doi:10.1179/107902611x13186000420242 · Cited by 598 · see citing works
Jones, D. A., Bigland-Ritchie, B., & Edwards, R. H. T. (1979) · Experimental Neurology · doi:10.1016/0014-4886(79)90279-6 · Cited by 596 · see citing works
Proprioceptive input resets central locomotor rhythm in the spinal cat
Conway, B. A., Hultborn, H., & Kiehn, O. (1987) · Experimental Brain Research · doi:10.1007/bf00249807 · Cited by 507 · see citing works
Robotic Orthosis Lokomat: a rehabilitation and research tool
Jezernik, S., Colombo, G., Keller, T., Frueh, H., & Morari, M. (2003) · Neuromodulation Technology at the Neural Interface · doi:10.1046/j.1525-1403.2003.03017.x · Cited by 503 · see citing works
Proprioception and locomotor disorders
Dietz, V. H. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn939 · Cited by 498 · see citing works
Donati, A. R. C., Shokur, S., Morya, E., Campos, D. S. F., Moioli, R. C., Gitti, C. M., Augusto, P. B., Tripodi, S., Pires, C. G., Pereira, G. A., et al. (2016) · Scientific Reports · doi:10.1038/srep30383 · Cited by 428 · see citing works
Self-citationBigland-Ritchie, B., Jones, D. A., & Woods, J. J. (1979) · Experimental Neurology · doi:10.1016/0014-4886(79)90280-2 · Cited by 351 · see citing works
Brain–machine interfaces in neurorehabilitation of stroke
Soekadar, S. R., Birbaumer, N., Slutzky, M. W., & Cohen, L. G. (2014) · Neurobiology of Disease · doi:10.1016/j.nbd.2014.11.025 · Cited by 335 · see citing works
Noninvasive Reactivation of Motor Descending Control after Paralysis
Gerasimenko, Y., Lu, D. C.-T., Modaber, M., Zdunowski, S., Gad, P. N., Sayenko, D. G., Morikawa, E., Haakana, P., Ferguson, A. R., Roy, R. R., et al. (2015) · Journal of Neurotrauma · doi:10.1089/neu.2015.4008 · Cited by 319 · see citing works
Functional Electrical Stimulation and rehabilitation—an hypothesis
Rushton, D. N. (2002) · Medical Engineering & Physics · doi:10.1016/s1350-4533(02)00040-1 · Cited by 308 · see citing works
Ragnarsson, K. T. (2007) · Spinal Cord · doi:10.1038/sj.sc.3102091 · Cited by 303 · see citing works
Behrman, A. L., Bowden, M. G., & Nair, P. M. (2006) · Physical Therapy · doi:10.2522/ptj.20050212 · Cited by 299 · see citing works
Dejnabadi, H., Jolles, B. M., & Aminian, K. (2005) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2005.851475 · Cited by 286 · see citing works
Hornby, T. G., Zemon, D. H., & Campbell, D. D. (2005) · Physical Therapy · doi:10.1093/ptj/85.1.52 · Cited by 284 · see citing works
Skeletal muscle fibre type transformation following spinal cord injury
Burnham, R. S., Martin, T. P., Stein, R. B., Bell, G. J., MacLean, I. M., & Steadward, R. D. (1997) · Spinal Cord · doi:10.1038/sj.sc.3100364 · Cited by 247 · see citing works
Kirshblum, S., Millis, S. R., McKinley, W. O., et al. (2004) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/j.apmr.2004.03.015 · Cited by 242 · see citing works
Model-based control of FES-induced single joint movements
Ferrarin, M., Palazzo, F., Riener, R., et al. (2001) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/7333.948452 · Cited by 234 · see citing works
Brain-Computer Interface in Stroke: A Review of Progress
Silvoni, S., Ramos‐Murguialday, A., Cavinato, M., Volpato, C., Cisotto, G., Turolla, A., Piccione, F., & Birbaumer, N. (2011) · Clinical EEG and Neuroscience · doi:10.1177/155005941104200410 · Cited by 225 · see citing works
Shindo, K., Kawashima, K., Ushiba, J., et al. (2011) · Journal of Rehabilitation Medicine · doi:10.2340/16501977-0859 · Cited by 216 · see citing works
Swinnen, E., Duerinck, S., Baeyens, J., et al. (2010) · Journal of Rehabilitation Medicine · doi:10.2340/16501977-0538 · Cited by 210 · see citing works
High accuracy decoding of user intentions using EEG to control a lower-body exoskeleton
Kilicarslan, A., Prasad, S., Grossman, R. G., & Contreras-Vidal, J. L. (2013) · Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC) · doi:10.1109/embc.2013.6610821 · Cited by 196 · see citing works
Rejc, E., Angeli, C. A., Atkinson, D., & Harkema, S. J. (2017) · Scientific Reports · doi:10.1038/s41598-017-14003-w · Cited by 180 · see citing works
Sherrick, C. E., & Rogers, R. (1966) · Perception & Psychophysics · doi:10.3758/bf03210054 · Cited by 169 · see citing works
Peckham, P. H., MORTIMER, J. T., & Marsolais, E. B. (1976) · Clinical Orthopaedics and Related Research · doi:10.1097/00003086-197601000-00041 · Cited by 164 · see citing works
Muscular, Skeletal, and Neural Adaptations Following Spinal Cord Injury
Shields, R. K. (2002) · Journal of Orthopaedic and Sports Physical Therapy · doi:10.2519/jospt.2002.32.2.65 · Cited by 159 · see citing works
Kokotilo, K. J., Eng, J. J., & Curt, A. E. P. (2009) · Journal of Neurotrauma · doi:10.1089/neu.2008.0688 · Cited by 157 · see citing works
Late recovery following spinal cord injury
McDonald, J. W., Becker, D., Sadowsky, C. L., Jane, J. A., Conturo, T. E., & Schultz, L. M. (2002) · Journal of Neurosurgery Spine · doi:10.3171/spi.2002.97.2.0252 · Cited by 154 · see citing works
Brain-controlled modulation of spinal circuits improves recovery from spinal cord injury
Bonizzato, M., Pidpruzhnykova, G., DiGiovanna, J., Shkorbatova, P., Pavlova, N., Micera, S., & Courtine, G. (2018) · Nature Communications · doi:10.1038/s41467-018-05282-6 · Cited by 149 · see citing works
Walking index for spinal cord injury (WISCI): criterion validation
Morganti, B., Scivoletto, G., Ditunno, P. L., et al. (2004) · Spinal Cord · doi:10.1038/sj.sc.3101658 · Cited by 148 · see citing works
Kapadia, N. M., Masani, K., Craven, B. C., Giangregorio, L., Hitzig, S. L., Richards, K., & Popović, M. R. (2014) · Journal of Spinal Cord Medicine · doi:10.1179/2045772314y.0000000263 · Cited by 131 · see citing works
ZeroG: Overground gait and balance training system
Hidler, J. M., Brennan, D., Black, I., Nichols, D., Brady, K., & Nef, T. (2011) · The Journal of Rehabilitation Research and Development · doi:10.1682/jrrd.2010.05.0098 · Cited by 127 · see citing works
Takahashi, M., Takeda, K., Otaka, Y., Osu, R., Hanakawa, T., Gouko, M., & Ito, K. (2012) · Journal of NeuroEngineering and Rehabilitation · doi:10.1186/1743-0003-9-56 · Cited by 127 · see citing works
Cortical sensorimotor reorganization after spinal cord injury
Green, J. B., Sora, E., Bialy, Y., Ricamato, A. L., & Thatcher, R. W. (1998) · Neurology · doi:10.1212/wnl.50.4.1115 · Cited by 126 · see citing works
Sadowsky, C. L., & McDonald, J. W. (2009) · Developmental Disabilities Research Reviews · doi:10.1002/ddrr.61 · Cited by 125 · see citing works
Malešević, N., Popović‐Maneski, L., Schwirtlich, L. B., & Popović, D. B. (2010) · Muscle & Nerve · doi:10.1002/mus.21736 · Cited by 116 · see citing works
Graupe, D., & Kohn, K. H. (1998) · Surgical Neurology · doi:10.1016/s0090-3019(98)00074-3 · Cited by 105 · see citing works
King, C., Wang, P. T., McCrimmon, C. M., Chou, C., Do, A. H., & Nenadić, Z. (2015) · Journal of NeuroEngineering and Rehabilitation · doi:10.1186/s12984-015-0068-7 · Cited by 104 · see citing works
Functional Electrical Stimulation in Spinal Cord Injury: From Theory to Practice
Martin, R. A., Sadowsky, C. L., Obst, K., et al. (2012) · Topics in Spinal Cord Injury Rehabilitation · doi:10.1310/sci1801-28 · Cited by 104 · see citing works
Tazoe, T., & Pérez, M. A. (2014) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/j.apmr.2014.07.418 · Cited by 93 · see citing works
Gurney‐Champion, O. J., Klaassen, R., Froeling, M., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0194590 · Cited by 81 · see citing works
Ragnarsson, K. T. (1988) · Clinical Orthopaedics and Related Research · doi:10.1097/00003086-198808000-00008 · Cited by 80 · see citing works
Musculoskeletal effects of an electrical stimulation induced cycling programme in the spinal injured
Sloan, K. E., Bremner, L. A., Byrne, J., Day, R. E., & Scull, E. R. (1994) · Spinal Cord · doi:10.1038/sc.1994.67 · Cited by 76 · see citing works
Lotze, M., Laubis‐Herrmann, U., Topka, H. R., et al. (1999) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-1999-00078 · Cited by 76 · see citing works
Raithatha, R., Carrico, C., Powell, E. S., Westgate, P. M., Chelette, K. C., Lee, K., Dunsmore, L., Salles, S. S., & Sawaki, L. A. (2016) · Neurorehabilitation · doi:10.3233/nre-151291 · Cited by 76 · see citing works
Restoration of gait by functional electrical stimulation for spinal cord injured patients
Gallien, P., Brissot, R., Eyssette, M., Tell, L., Barat, M., Wiart, L., & Petit, K. (1995) · Spinal Cord · doi:10.1038/sc.1995.138 · Cited by 74 · see citing works
Shokur, S., Gallo, S., Moioli, R. C., Donati, A. R. C., Morya, E., Bleuler, H., & Nicolelis, M. A. L. (2016) · Scientific Reports · doi:10.1038/srep32293 · Cited by 74 · see citing works
Self-citationFunctional electrical stimulation (FES): muscle histochemical analysis
Greve, J. M. D., Muszkat, R., Schmidt, B., Chiovatto, J., Filho, T. E. P. D. B., & Battistella, L. R. (1993) · Spinal Cord · doi:10.1038/sc.1993.119 · Cited by 54 · see citing works
Brain–Computer Interfaces in the Rehabilitation of Stroke and Neurotrauma
Soekadar, S. R., Birbaumer, N., & Cohen, L. G. (2011) · Springer eBooks · doi:10.1007/978-4-431-54008-3_1 · Cited by 50 · see citing works
Measurement of circumference of the knee with ordinary tape measure.
Nicholas, J. J., Taylor, F. H., Buckingham, R. B., & Ottonello, D. (1976) · Annals of the Rheumatic Diseases · doi:10.1136/ard.35.3.282 · Cited by 49 · see citing works
Shokur, S., Donati, A., Campos, D., Gitti, C. M., Bao, G., Fischer, D., Almeida, S., Braga, V. A. S., Augusto, P., Petty, C., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0206464 · Cited by 44 · see citing works
Self-citationBeaumont, É., Guevara, E., Dubeau, S., Lesage, F., Nagai, M. K., & Popović, M. R. (2013) · Journal of Spinal Cord Medicine · doi:10.1179/2045772313y.0000000117 · Cited by 34 · see citing works
A Study of a Knee Extension Controlled by a Closed Loop Functional Electrical Stimulation
Schmitt, C., & Métrailler, P. (2004) · Infoscience (Ecole Polytechnique Fédérale de Lausanne) · Cited by 24 · see citing works
Popović, M. R., Masani, K., & Micera, S. (2011) · Springer eBooks · doi:10.1007/978-1-4471-2277-7_7 · Cited by 22 · see citing works
Robotics 2010 Current and Future Challenges
Abdellatif, H. (2010) · InTech eBooks · doi:10.5772/142 · Cited by 13 · see citing works
Yves, S., Bouri, M., Clavel, R., et al. (2010) · InTech eBooks · doi:10.5772/7328 · Cited by 11 · see citing works
Self-citationKo, C., Chang, Y., Kim, S., Kim, S.-K., Kim, G., Ryu, J., & Mun, M.-S. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.10.021 · Cited by 8 · see citing works
Système robotique pour la mobilisation des membres inférieurs d'une personne paraplégique
Métrailler, P. (2005) · Infoscience (Ecole Polytechnique Fédérale de Lausanne) · doi:10.5075/epfl-thesis-3191 · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Walking naturally after spinal cord injury using a brain–spine interface
Lorach, H., Galvez, A., Spagnolo, V., Martel, F., Karakas, S., Intering, N., Vat, M., Faivre, O., Harte, C., Komi, S., et al. (2023) · Nature · doi:10.1038/s41586-023-06094-5 · Cited by 631 · see citing works
“Comparable observations have been reported when electroencephalographic signals were coupled to an exoskeleton or functional electrical stimulation of muscles during gait rehabilitation in people with spinal cord injury 22,24,35 .”
Background
- Authors
- Selfslagh, A., Shokur, S., Campos, D. S. F., Donati, A. R. C., Almeida, S., Yamauti, S. Y., Coelho, D. B., Bouri, M., & Nicolelis, M. A. L.
- Affiliations
- École Polytechnique Fédérale de Lausanne (CH)
- Associação de Assistência à Criança Deficiente (BR)
- Universidade Federal do ABC (BR)
- Duke University (US)
- Corresponding author
- Nicolelis, Miguel A. L.
- Venue
- Scientific Reports
- Published
- 2019-05-01
- Volume
- 9
- Issue
- 1
- Pages
- 6782-6782
- ISSN
- 2045-2322 (ISSN-L)
- PMC
- PMC6494802
- OpenAlex
- W2942835517
- Cited by
- 78
- References
- 73
- Citations by year
- 2026: 4 · 2025: 16 · 2024: 8 · 2023: 6 · 2022: 19 · 2021: 13 · 2020: 10 · 2019: 2
- FWCI
- 8.10
- Type
- journal article
- Language
- en
- Update notices
- correction (2019-12-04)
- Open access
- gold
- doi.org
- Locations
- Scientific Reports (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
- Funders
- Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
- Ministério da Ciência, Tecnologia e Inovação
- Conselho Nacional de Desenvolvimento Científico e Tecnológico
- Financiadora de Estudos e Projetos
- Fundação de Apoio à Pesquisa do Rio Grande do Norte
- Topics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Spinal Cord Injury Research
- Health Sciences › Medicine › Rehabilitation › Stroke Rehabilitation and Recovery
- Physical Sciences › Engineering › Biomedical Engineering › Prosthetics and Rehabilitation Robotics
- Keywords
- spinal cord injury, paraplegia, brain-computer interface, motor imagery, gait training, body weight support, proprioceptive feedback, tactile feedback, balance control, neurorehabilitation
- MeSH terms
- Neurological Rehabilitation, Adult, Brain, Electric Stimulation Therapy, Exercise Therapy, Gait, Humans, Locomotion, Paraplegia, Spinal Cord Injuries, Walking
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
